7-Tesla evidence for columnar and rostral-caudal organization of the human periaqueductal gray response in the absence of threat: a working memory study.

The periaqueductal gray (PAG) is a small midbrain structure that surrounds the cerebral aqueduct, regulates brain-body communication, and is often studied for its role in "fight-or-flight" and "freezing" responses to threat. We used ultra-high field 7-Tesla fMRI to resolve the PAG in humans and distinguish it from the cerebral aqueduct, examining its in vivo function in humans during a working memory task (N = 87). Both mild and moderate cognitive demand elicited spatially similar patterns of whole brain BOLD response, and moderate cognitive demand elicited widespread BOLD increases above baseline in the brainstem. Notably, these brainstem increases were not significantly greater than those in the mild demand condition, suggesting that a subthreshold brainstem BOLD increase occurred for mild cognitive demand as well. PAG response was group-aligned and examined with subject-specific masks. In PAG, both mild and moderate demand elicited a well-defined response in ventrolateral PAG (vlPAG), a region thought to be functionally related to anticipated painful threat in humans and non-human animals-yet, the present task posed only the most minimal (if any) "threat", with the cognitive tasks used being approximately equivalent to remembering a phone number. These findings suggest that the PAG may play a more general role in visceromotor regulation, even in the absence of threat.Significance statement The periaqueductal gray (PAG) is thought to control survival-related behavior, and is typically studied using experiments that manipulate threat. Others have proposed that the PAG plays a more general role in bodily regulation, but studies examining PAG function outside of threat-based experimental contexts are rare. We used high-resolution fMRI to examine PAG response in humans during a working memory task, which involves minimal threat. Moderate cognitive demands elicited a well-defined response in ventrolateral PAG, a functional subregion thought to coordinate a "freezing" response to threat. A task where threat is minimal elicited a clear fMRI response in one of the most well-known survival circuits in the brain, which suggests the PAG supports a more general function in brain--body coordination.

Semantic Clustering during Verbal Episodic Memory Encoding and Retrieval in Older Adults: One Cognitive Mechanism of Superaging.

Normal aging is commonly accompanied by a decline in cognitive abilities, including memory, yet some individuals maintain these abilities as they get older. We hypothesize that semantic clustering, as an effective strategy for improving performance on episodic recall tasks, may contribute to the maintenance of youthful memory in older adults. We investigated the dynamics of spontaneous production and utilization of the semantic clustering strategy in two independent samples of older adults who completed a list learning paradigm (N1 = 40 and N2 = 29, respectively). Specifically, we predicted and observed that older adults who spontaneously used a semantic clustering strategy throughout the encoding process learned more words by the culmination of the encoding trials (Sample 1, R2= 0.53, p < 0.001; Sample 2, R2= 0.51, p < 0.001), and that those who utilized this strategy during retrieval recalled more words, when compared to older adults who did not produce or utilize a semantic clustering strategy during both a short (Sample 1, R2 = 0.81, p < 0.001; Sample 2, R2 = 0.70, p < 0.001) and long delay retrieval (Sample 1, R2 = 0.83, p < 0.001; Sample 2, R2 = 0.77, p < 0.001). We further predicted and observed that older adults who maintained a youthful level of delayed free recall (i.e., "Superagers") produced (Sample 1, F(1, 38) = 17.81, p < 0.0001; Sample 2, F(1, 27) = 14.45, p < 0.0001) and utilized (Sample 1, F(1, 39) = 25.84, p < 0.0001; Sample 2, F(1, 27) = 12.97, p < 0.01) more semantic clustering than did older individuals with normal memory for their age. These results suggest one cognitive mechanism through which Superagers maintain youthful memory function and raise the possibility that older adults may be able to train themselves to use strategies to promote better memory.

What We Can Learn About Emotion by Talking With the Hadza.

Emotions are often thought of as internal mental states centering on individuals' subjective feelings and evaluations. This understanding is consistent with studies of emotion narratives, or the descriptions people give for experienced events that they regard as emotions. Yet these studies, and contemporary psychology more generally, often rely on observations of educated Europeans and European Americans, constraining psychological theory and methods. In this article, we present observations from an inductive, qualitative analysis of interviews conducted with the Hadza, a community of small-scale hunter-gatherers in Tanzania, and juxtapose them with a set of interviews conducted with Americans from North Carolina. Although North Carolina event descriptions largely conformed to the assumptions of eurocentric psychological theory, Hadza descriptions foregrounded action and bodily sensations, the physical environment, immediate needs, and the experiences of social others. These observations suggest that subjective feelings and internal mental states may not be the organizing principle of emotion the world around. Qualitative analysis of emotion narratives from outside of a U.S. (and western) cultural context has the potential to uncover additional diversity in meaning-making, offering a descriptive foundation on which to build a more robust and inclusive science of emotion.

Adaptive thresholding increases sensitivity to detect changes in the rate of skin conductance responses to psychologically arousing stimuli in both laboratory and ambulatory settings.

Psychophysiologists recording electrodermal activity (EDA) often derive measures of slow, tonic activity-skin conductance level (SCL)-and faster, more punctate changes-skin conductance responses (SCRs). A SCR is conventionally considered to have occurred when the local amplitude of the EDA signal exceeds a researcher-determined threshold (e.g., 0.05 µS), typically fixed across study participants and conditions. However, fixed SCR thresholds can preferentially exclude data from individuals with low SCL because their SCRs are smaller on average, thereby reducing statistical power for group-level analyses. Thus, we developed a fixed plus adaptive (FA) thresholding method that adjusts identification of SCRs based on an individual's SC at the onset of the SCR to increase statistical power and include data from more participants. We assess the utility of applying FA thresholding across two independent samples and explore age and race-related associations with EDA outcomes. Study 1 uses wired EDA measurements from 254 healthy adults responding to evocative images and sounds in a laboratory setting. Study 2 uses wireless EDA measurements from 20 children with autism in a clinical environment while they completed behavioral tasks. Compared to a 0.01, 0.03, and 0.05 µS fixed threshold, FA thresholding at 1.9% modestly increases statistical power to detect a difference in SCR rate between tasks with higher vs. lower subjective arousal and reduces exclusion of participants by up to 5% across both samples. This novel method expands the EDA analytical toolbox and may be useful in populations with highly variable basal SCL or when comparing groups with different basal SCL. Future research should test for reproducibility and generalizability in other tasks, samples, and contexts. IMPACT STATEMENTS: This article is important because it introduces a novel method to enhance sensitivity and statistical power in analyses of skin conductance responses from electrodermal data.

Multimodal, Idiographic Ambulatory Sensing Will Transform our Understanding of Emotion.

Emotions are inherently complex - situated inside the brain while being influenced by conditions inside the body and outside in the world - resulting in substantial variation in experience. Most studies, however, are not designed to sufficiently sample this variation. In this paper, we discuss what could be discovered if emotion were systematically studied within persons 'in the wild', using biologically-triggered experience sampling: a multimodal and deeply idiographic approach to ambulatory sensing that links body and mind across contexts and over time. We outline the rationale for this approach, discuss challenges to its implementation and widespread adoption, and set out opportunities for innovation afforded by emerging technologies. Implementing these innovations will enrich method and theory at the frontier of affective science, propelling the contextually situated study of emotion into the future.

A functional account of stimulation-based aerobic glycolysis and its role in interpreting BOLD signal intensity increases in neuroimaging experiments.

In aerobic glycolysis, oxygen is abundant, and yet cells metabolize glucose without using it, decreasing their ATP per glucose yield by 15-fold. During task-based stimulation, aerobic glycolysis occurs in localized brain regions, presenting a puzzle: why produce ATP inefficiently when, all else being equal, evolution should favor the efficient use of metabolic resources? The answer is that all else is not equal. We propose that a tradeoff exists between efficient ATP production and the efficiency with which ATP is spent to transmit information. Aerobic glycolysis, despite yielding little ATP per glucose, may support neuronal signaling in thin (< 0.5 µm), information-efficient axons. We call this the efficiency tradeoff hypothesis. This tradeoff has potential implications for interpretations of task-related BOLD "activation" observed in fMRI. We hypothesize that BOLD "activation" may index local increases in aerobic glycolysis, which support signaling in thin axons carrying "bottom-up" information, or "prediction error"-i.e., the BIAPEM (BOLD increases approximate prediction error metabolism) hypothesis. Finally, we explore implications of our hypotheses for human brain evolution, social behavior, and mental disorders.

Cortical and subcortical mapping of the allostatic-interoceptive system in the human brain: replication and extension with 7 Tesla fMRI.

The brain continuously anticipates the energetic needs of the body and prepares to meet those needs before they arise, a process called allostasis. In support of allostasis, the brain continually models the internal state of the body, a process called interoception. Using published tract-tracing studies in non-human animals as a guide, we previously identified a large-scale system supporting allostasis and interoception in the human brain with functional magnetic resonance imaging (fMRI) at 3 Tesla. In the present study, we replicated and extended this system in humans using 7 Tesla fMRI (N = 91), improving the precision of subgenual and pregenual anterior cingulate topography as well as brainstem nuclei mapping. We verified over 90% of the anatomical connections in the hypothesized allostatic-interoceptive system observed in non-human animal research. We also identified functional connectivity hubs verified in tract-tracing studies but not previously detected using 3 Tesla fMRI. Finally, we demonstrated that individuals with stronger fMRI connectivity between system hubs self-reported greater interoceptive awareness, building on construct validity evidence from our earlier paper. Taken together, these results strengthen evidence for the existence of a whole-brain system supporting interoception in the service of allostasis and we consider the implications for mental and physical health.

Signal processing in the vagus nerve: Hypotheses based on new genetic and anatomical evidence.

Each organism must regulate its internal state in a metabolically efficient way as it interacts in space and time with an ever-changing and only partly predictable world. Success in this endeavor is largely determined by the ongoing communication between brain and body, and the vagus nerve is a crucial structure in that dialogue. In this review, we introduce the novel hypothesis that the afferent vagus nerve is engaged in signal processing rather than just signal relay. New genetic and structural evidence of vagal afferent fiber anatomy motivates two hypotheses: (1) that sensory signals informing on the physiological state of the body compute both spatial and temporal viscerosensory features as they ascend the vagus nerve, following patterns found in other sensory architectures, such as the visual and olfactory systems; and (2) that ascending and descending signals modulate one another, calling into question the strict segregation of sensory and motor signals, respectively. Finally, we discuss several implications of our two hypotheses for understanding the role of viscerosensory signal processing in predictive energy regulation (i.e., allostasis) as well as the role of metabolic signals in memory and in disorders of prediction (e.g., mood disorders).

Heightened fearfulness in infants is not adaptive.

Grossmann proposes the "fearful ape hypothesis," suggesting that heightened fearfulness in early life is evolutionarily adaptive. We question this claim with evidence that (1) perceived fearfulness in children is associated with negative, not positive long-term outcomes; (2) caregivers are responsive to all affective behaviors, not just those perceived as fearful; and (3) caregiver responsiveness serves to reduce perceived fearfulness.

Correspondence of functional connectivity gradients across human isocortex, cerebellum, and hippocampus.

Gradient mapping is an important technique to summarize high dimensional biological features as low dimensional manifold representations in exploring brain structure-function relationships at various levels of the cerebral cortex. While recent studies have characterized the major gradients of functional connectivity in several brain structures using this technique, very few have systematically examined the correspondence of such gradients across structures under a common systems-level framework. Using resting-state functional magnetic resonance imaging, here we show that the organizing principles of the isocortex, and those of the cerebellum and hippocampus in relation to the isocortex, can be described using two common functional gradients. We suggest that the similarity in functional connectivity gradients across these structures can be meaningfully interpreted within a common computational framework based on the principles of predictive processing. The present results, and the specific hypotheses that they suggest, represent an important step toward an integrative account of brain function.

Improving the study of brain-behavior relationships by revisiting basic assumptions.

Neuroimaging research has been at the forefront of concerns regarding the failure of experimental findings to replicate. In the study of brain-behavior relationships, past failures to find replicable and robust effects have been attributed to methodological shortcomings. Methodological rigor is important, but there are other overlooked possibilities: most published studies share three foundational assumptions, often implicitly, that may be faulty. In this paper, we consider the empirical evidence from human brain imaging and the study of non-human animals that calls each foundational assumption into question. We then consider the opportunities for a robust science of brain-behavior relationships that await if scientists ground their research efforts in revised assumptions supported by current empirical evidence.

The Qwantify app dataset: A remote experience sampling study of desire, emotion, and well-being.

Experiences of desire-the feeling of wanting to have, do, or experience something-are pervasive and varied. Recent theoretical advances draw attention to characterizing this variation. Thus, this study investigated experiences of desire in everyday life and co-occurring social, physical, and emotional states, including facets of emotional experiences known to be related to well-being (e.g., perceived loneliness and stress). The Qwantify app was designed to run a remote experience sampling study. Through the app, participants were randomly alerted during their daily life to report on their experience in the moment. During the data collection period, any individual could download the freely available Qwantify app and participate in the study, without providing identifying information or communicating with researchers. Similar to other remote experience sampling studies, an incentive for participants to engage in the study was unlocking visualizations of their own data. Over 600 participants downloaded the app, completed the sign-up process, and responded to at least one experience sampling alert. Approximately 40% of these participants went on to respond to 50 alerts. The purpose of this report is to describe this experience sampling dataset such that it can be used to test a variety of hypotheses, including hypotheses regarding individual differences.

Context reconsidered: Complex signal ensembles, relational meaning, and population thinking in psychological science.

This article considers the status and study of "context" in psychological science through the lens of research on emotional expressions. The article begins by updating three well-trod methodological debates on the role of context in emotional expressions to reconsider several fundamental assumptions lurking within the field's dominant methodological tradition: namely, that certain expressive movements have biologically prepared, inherent emotional meanings that issue from singular, universal processes which are independent of but interact with contextual influences. The second part of this article considers the scientific opportunities that await if we set aside this traditional understanding of "context" as a moderator of signals with inherent psychological meaning and instead consider the possibility that psychological events emerge in ecosystems of signal ensembles, such that the psychological meaning of any individual signal is entirely relational. Such a fundamental shift has radical implications not only for the science of emotion but for psychological science more generally. It offers opportunities to improve the validity and trustworthiness of psychological science beyond what can be achieved with improvements to methodological rigor alone. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Erratum: Publisher Correction: Assessing the Power of Words to Facilitate Emotion Category Learning.

[This corrects the article DOI: 10.1007/s42761-021-00084-4.].

Affect and Social Judgment: The Roles of Physiological Reactivity and Interoceptive Sensitivity.

Humans imbue the objects of their perception with affective meaning, a phenomenon called affective realism. The affective realism hypothesis proposes that a brain continually predicts the meaning of sensations (e.g., identifying a sound as a siren, or a visual array as a face) in part by representing the current state of the body and the immediate physiological impact that similar sensory events have entailed in the past. However, the precise contribution of physiological activity to experiences of affective realism remains unknown. In the present study, participants' peripheral physiological activity was recorded while they made social evaluative judgments of target faces displaying neutral expressions. Target faces were shown concurrent with affective images that were suppressed from reportable awareness using continuous flash suppression. Results revealed evidence of affective realism-participants judged target faces more positively when paired with suppressed positive stimuli than suppressed negative stimuli-but this effect was significantly less pronounced among individuals higher in cardiac interoceptive sensitivity. Moreover, while some modest differences in peripheral physiological activity were observed across suppressed affective stimulus conditions, physiological reactivity to affective stimuli did not directly predict social evaluative judgments. We explore the implications of these findings with respect to both theories of emotion and theories detailing a role for interoception in experiences of first-person subjectivity. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-022-00114-9.

Assessing the Power of Words to Facilitate Emotion Category Learning.

Previous research suggests that labels shape the categorization of emotional stimuli such as facial configurations, yet the strongest evidence of labels' influence on category learning comes from work on object categories. In particular, Lupyan et al. (Psychol Sci 18(12):1077-1083, 2007) found that novel categories of aliens were learned faster by participants provided with nonsense labels during feedback. We summarize a series of five studies in which we examined whether this word-enhancement effect on learning would extend to novel categories of emotion. These studies were conceptual replications of the paradigm used by Lupyan et al. (Psychol Sci 18(12):1077-1083, 2007) designed so that participants would associate novel expressive behaviors with situated experiences. We hypothesized that participants would learn to categorize exemplars of novel emotion categories over the duration of the task, and that categorization would be facilitated for participants who were presented with category labels during learning. We simultaneously analyzed data from all five studies in an integrative data analysis, allowing us to test the effects of learning over time and label condition with increased statistical power. Across all five studies, we found that, while participant performance did improve over time, in no case was it facilitated by including emotion labels at feedback. These results join others in suggesting that the effect of labels on emotion categorization may be more context-dependent than previously supposed-varying by the type of category learning task as well as the specific categories being learned and their relationship to previously acquired knowledge-such that there may be multiple pathways for emotion category learning. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-021-00084-4.

Structural integrity of the anterior mid-cingulate cortex contributes to resilience to delirium in SuperAging.

Despite its devastating clinical and societal impact, approaches to treat delirium in older adults remain elusive, making it important to identify factors that may confer resilience to this syndrome. Here, we investigated a cohort of 93 cognitively normal older patients undergoing elective surgery recruited as part of the Successful Aging after Elective Surgery study. Each participant was classified either as a SuperAger (n = 19) or typically aging older adult (n = 74) based on neuropsychological criteria, where the former was defined as those older adults whose memory function rivals that of young adults. We compared these subgroups to examine the role of preoperative memory function in the incidence and severity of postoperative delirium. We additionally investigated the association between indices of postoperative delirium symptoms and cortical thickness in functional networks implicated in SuperAging based on structural magnetic resonance imaging data that were collected preoperatively. We found that SuperAging confers the real-world benefit of resilience to delirium, as shown by lower (i.e. zero) incidence of postoperative delirium and decreased severity scores compared with typical older adults. Furthermore, greater baseline cortical thickness of the anterior mid-cingulate cortex-a key node of the brain's salience network that is also consistently implicated in SuperAging-predicted lower postoperative delirium severity scores in all patients. Taken together, these findings suggest that baseline memory function in older adults may be a useful predictor of postoperative delirium risk and severity and that superior memory function may contribute to resilience to delirium. In particular, the integrity of the anterior mid-cingulate cortex may be a potential biomarker of resilience to delirium, pointing to this region as a potential target for preventive or therapeutic interventions designed to mitigate the risk or consequences of developing this prevalent clinical syndrome.

A new science of emotion: implications for functional neurological disorder.

Functional neurological disorder reflects impairments in brain networks leading to distressing motor, sensory and/or cognitive symptoms that demonstrate positive clinical signs on examination incongruent with other conditions. A central issue in historical and contemporary formulations of functional neurological disorder has been the mechanistic and aetiological role of emotions. However, the debate has mostly omitted fundamental questions about the nature of emotions in the first place. In this perspective article, we first outline a set of relevant working principles of the brain (e.g. allostasis, predictive processing, interoception and affect), followed by a focused review of the theory of constructed emotion to introduce a new understanding of what emotions are. Building on this theoretical framework, we formulate how altered emotion category construction can be an integral component of the pathophysiology of functional neurological disorder and related functional somatic symptoms. In doing so, we address several themes for the functional neurological disorder field including: (i) how energy regulation and the process of emotion category construction relate to symptom generation, including revisiting alexithymia, 'panic attack without panic', dissociation, insecure attachment and the influential role of life experiences; (ii) re-interpret select neurobiological research findings in functional neurological disorder cohorts through the lens of the theory of constructed emotion to illustrate its potential mechanistic relevance; and (iii) discuss therapeutic implications. While we continue to support that functional neurological disorder is mechanistically and aetiologically heterogenous, consideration of how the theory of constructed emotion relates to the generation and maintenance of functional neurological and functional somatic symptoms offers an integrated viewpoint that cuts across neurology, psychiatry, psychology and cognitive-affective neuroscience.

Allostasis, Action, and Affect in Depression: Insights from the Theory of Constructed Emotion.

The theory of constructed emotion is a systems neuroscience approach to understanding the nature of emotion. It is also a general theoretical framework to guide hypothesis generation for how actions and experiences are constructed as the brain continually anticipates metabolic needs and attempts to meet those needs before they arise (termed allostasis). In this review, we introduce this framework and hypothesize that allostatic dysregulation is a trans-disorder vulnerability for mental and physical illness. We then review published findings consistent with the hypothesis that several symptoms in major depressive disorder (MDD), such as fatigue, distress, context insensitivity, reward insensitivity, and motor retardation, are associated with persistent problems in energy regulation. Our approach transforms the current understanding of MDD as resulting from enhanced emotional reactivity combined with reduced cognitive control and, in doing so, offers novel hypotheses regarding the development, progression, treatment, and prevention of MDD.

Emotion and threat detection: The roles of affect and conceptual knowledge.

Prior research has demonstrated that angry participants exhibit biased threat detection whereby they are more likely to misidentify neutral objects as guns. Yet, it is unclear whether independent components of anger, such as conceptual knowledge about anger or the affective features of an anger instance, could lead to altered bias alone. Consistent with constructionist theories of emotion, the present set of two experiments demonstrates that threat-detection bias only differs significantly between participants in an emergent-anger condition, who had engaged both components of anger (i.e., conceptual knowledge of anger and negative, high arousal affect), and participants in a control condition, who had engaged neither. Study 2 demonstrates that this pattern of findings also extends to another threat-relevant emotional state (i.e., fear). Implications for studying anger and fear, and emotions more generally, as constructed mental experiences are discussed. (PsycInfo Database Record (c) 2022 APA, all rights reserved).